Classification of Vascular Plants in Vietnam According to Modern Classification Systems

Vietnam is extremely rich in biodiversity, with a remarkable range of habitats and more than 13,500 species of vascular plants recorded for the flora of Vietnam. This number represents about 3 to 5% of the world’s diversity of vascular plants. Over the past 30 years, there were two important documents on the vascular plants of Vietnam published, An Illustrated Flora of Vietnam (IFV) and Checklist of Plant Species of Vietnam (CPSV). During the past half century, the advent of molecular phylogenetics has witnessed dramatic changes in the classifications of vascular plants, and some modern classification systems of vascular plants have been established, e.g., PPG I, GPG, and APG. However, the vascular plants of Vietnam have not yet been classified according to these modern classification systems. In this paper, we present the history of the classification of vascular plants in Vietnam, compare the circumscription of all families of vascular plants occurring within Vietnam in IFV, CPSV, and the modern classification systems when applicable, and summarize familial assignments of all controversial genera in the different classifications. Furthermore, we also arrange the 37 families of lycophytes and ferns occurring within Vietnam according to the latest classification system (PPG I) and the 8 families of gymnosperms according to the latest Christenhusz’s system (GPG). The 246 families of angiosperms are arranged according to the fourth edition of the latest Angiosperm Phylogeny Group (APG IV). These results are the foundation stones and would be helpful for future research on the flora of Vietnam and the arrangement of plant collections in Vietnamese herbaria based on the updated classifications.


Introduction
Vietnam is one of the most biodiverse countries, with a huge variety of distinctive and fascinating wildlife. It is adjacent with the natural geography of southern China, where the diversity of extant vascular plants is extraordinary [1]. The flora of Vietnam is also rich in species composition, with more than 20,000 plant species recorded [2], containing many endemic taxa and key and primitive taxa of angiosperm phylogeny, possibly the origin of East Asian flora, and even angiosperms [3]. Therefore, Vietnam is a significant bioregional area in terms of physical geography and biogeography, necessitating biodiversity conservation.
Biological classifications are fundamental tools for communication about biodiversity [4]. The stability of names is thus of great importance, and it is critical to consider existing classifications when determining taxa worthy of recognition and the ranks at which to treat them. A focus on natural groups is similarly essential, as it results in classifications that reflect the evolutionary history and ultimately lead to greater stability. Nowadays, the surge in the application of molecular biology techniques has resulted in significant

History of Classification of Vascular Plants in Vietnam
Vascular plant species of Vietnam have been initially documented since the beginning of the 18th century by French botanists from the Museum National d'Histoire Naturelle, Paris. They began with the flora of the southern parts of the country. João de Loureiro (1710-1791) initially studied and wrote the first one, Flora Cochinchinensis (in Latin), including Vols. 1-2 [11]. Loureiro's work was an extension of his interest in local medicinal plants, in the service of the King of Cochinchina, a region in the southern third of modern Vietnam that included Ho Chi Minh city and Thua Thien Hue province, and at some later point, a French colony. Loureiro's specimen collections, which would have been important reference material, and his plant descriptions were very brief. His work was followed by Pierre Louis (1833Louis ( -1905, who published 26 parts bound in 4 volumes of Flore forestière de la Cochinchine (in French) [19] Later, Francois Gagnepain (1866Gagnepain ( -1952, Henri Lecomte  , and Henri Humbert (1887-1967) published Flore générale de l'Indo-Chine (FGIC), comprising Vols. 1-7, for the three countries of the Indochinese region: Vietnam, Laos, and Cambodia [12]. The families in Flore générale de l'Indo-Chine were classified according to "Le Genera Plantarum" [20].
While revising the previous treatments for the floras of Vietnam, Laos, and Cambodia, plant taxonomists from the Museum National d'Histoire Naturelle, Paris, and domestic taxonomists [11,12,19] compiled Flore du Cambodge, du Laos et du Viêtnam in French (FCLV), a project begun by André Aubréville in 1960 to succeed Flore générale de l'Indochine, coordinated by H. Lecomte and H. Humbert during 1907-1934, and H. Humbert until 1951 [12]. That last issue was Vol. 32 in 2004 for Myrsinaceae. The whole project consists of 32 volumes, dealing with 1552 species in 77 families of vascular plants [13], of which 69 families in 31 volumes are angiosperms; only 1 volume (Vol. 28) is for 8 families of the gymnosperms. None of the fern and lycophyte families were treated.
Since 2013, the series has been renewed in the English-language version as The Flora of Cambodia, Laos, and Vietnam and jointly co-published by the Museum National d'Histoire Naturelle, Paris, and the Royal Botanic Garden of Edinburgh. This book series is considered to be an ongoing project. The most recently published volumes were Vol. 33 for Apocynaceae [21], Vol. 34 for Polygonaceae [22], Vol. 35 for Solanaceae [23], and Vol. 36 for Convolvulaceae [24]. Several volumes are still in revision, and more volumes will come out in the future. So far, not many species and families are recorded in each volume, far from the total number of vascular plants in these three countries in general and Vietnam in particular.
None of the families of the ferns, lycophytes, and gymnosperms have been published in the FOV. Therefore, representation of the entirety of flora is still lacking in coverage of the total number of vascular plant families in the country.
Pham Hoang Ho (1929-2017) originally published Illustrated Flora of Southern Vietnam with the support of the South Vietnamese Ministry of Education in 1969 [14]. Its second edition was published in two volumes in 1970 and 1972, respectively. Later, more plant species from Northern Vietnam were added to the last edition [15]. Therefore, it was revised in a new version, An Illustrated Flora of Vietnam (Cây cỏ Việt Nam) (IFV). The first edition included three volumes in Vietnamese [16]. The last edition also published 3 volumes in Vietnamese, which documented 11,611 species, 2249 genera, and 284 families of vascular plants, of which 139 genera and 33 families are ferns and lycophytes, 25 genera and 10 families are gymnosperms, and the rest are genera and families of angiosperms [17]. Each species includes nomenclature, a brief description, and a simple line drawing. The book is currently relatively complete, so the usage rate is relatively high by both foreign and Vietnamese botanists to identify plants. Although the classification system and delimitation of families and genera of vascular plants in the book were not mentioned, they were probably adopted from the previous treatments by French botanists [11][12][13].
Based on various published documents in Vietnam, as well as neighboring countries, such as China, Thailand, Laos, and Cambodia, and non-published materials by Vietnamese, botanists completed a Checklist of Plant Species of Vietnam (CPSV). The working group was comprised of more than 40 botanists from the Institute of Ecology and Biological Resource (IEBR), Vietnam Academy of Science and Technology, Center for Natural Resources and Environmental Studies (CRES), and Vietnam National University in Hanoi, in collaboration with some Russian botanists. The completed Checklist of Plant Species of Vietnam (CPSV) from Procaryophyta, Fungi, and Algae to Angiospermae, was divided into three volumes. The first volume (Vol. 1) is composed of phylum from Procaryota to Gymnospermae and part of angiosperms, while the two other volumes (Vols. 2 & 3) are exclusively for the rest of the Angiospermae in Vietnam [2]. For the angiosperms, the delimitation of the families was mainly adopted from previous work [18], which classified the angiosperms in Vietnam following Takhtajan's classification systems [28,29]. Species are assigned to genera and families according to the Kew Herbarium Concept [51]. By family, each species includes full nomenclature and a brief description of morphology, distribution, some ecological features, and their use or harm. These three volumes documented 11,550 species and subspecies of 2374 genera, and 308 families of vascular plants in Vietnam. Of this total, 700 species and subspecies of 143 genera and 34 families are ferns and lycophytes, 70 species, and subspecies of 21 genera and 9 families are gymnosperms, and 10,780 species and subspecies of 2210 genera and 265 families are Angiospermae.

Classification of Vascular Plants of Vietnam according to Modern Classification Systems
The comparison of circumscription and classification of vascular plants of Vietnam in IFV, CPSV, and PPG 1 (for lycophytes and ferns), GPG (for gymnosperms), and APG IV (for angiosperms), is presented in the seven following tables (please see the Supplementary Materials).

Lycophytes and Ferns
For the lycophytes and ferns of Vietnam (Tables S1 and S4), IFV (Vol. 1) recognized 139 genera and 33 families, while CPSV (Vol. 1) recognized 143 genera and 34 families. The delimitation of genera and families in both IFV and CPSV is the same, with 28 out of the 33 families of lycophytes and ferns in IFV having the exact delimitation as CPSV (Table S1). These 28 families are morphologically homogenous, and the circumscription of these families has rarely been controversial [9,52].
However, the delimitation of some genera and families is different between IFV and CPSV. The family Oleandraceae (incl. Arthropteris, Nephrolepis, and Oleandra) sensu CPSV was not recognized in IFV. The only member of Thyrsopteridaceae (Cibotium) sensu IFV is accommodated in Dicksoniaceae in CPSV; Angiopteris and Archangiopteris (Angiopteridaceae) sensu IFV were transferred to Marattiaceae in CPSV; and some genera (Athyrium, Cystopteris, Diplazium) of Aspleniaceae sensu IFV were transferred to Woodsiaceae in CPSV, which was not recognized in IFV.
Based on the previous study [52], Phan [53] classified all species of ferns from Vietnam, but not including lycophytes, into 135 genera, 28 families, 11 orders, and 4 classes, of which 3 families (Lindsaeaceae, Cibotaceae, and Lygodiaceae) are newly circumscribed for Vietnam (Tables S1 and S4). The results showed that Ophioglossaceae belonging to Polypodiophyta was transferred to another class, Psilotopsida; especially Marattiaceae belonging to Polypodiophyta was split into its own class, namely, Marattiopsida. Three families sensu IFV and CPSV were merged with other families in Phan, suggesting that the circumscription of these three families is broader than the corresponding families recognized in IFV and CPSV. Indeed, based on chloroplast sequence data, some families, sensu IFV and CPSV, were merged in Phan, and are apparently monophyletic, but nested within other families, e.g., Azollaceae (in Salviniaceae [54]) and Cheiropleuriaceae (in Dipteridaceae [55]).
According to PPG I [9], the lycophytes and ferns of Vietnam were classified into 2 classes, 3 sub-classes, 14 orders, 37 families, and 134 genera. By following this modern classification, the families of lycophytes and ferns in Vietnam are more than the previous treatments [2,17,53], of which six families (Cystopteridaceae, Rhachidosaraceae, Diplaziopsidaceae, Didymochlaenaceae, Hypodematiaceae, and Nephrolepidaceae) were newly circumscribed for Flora of Vietnam, but its number of genera is less than those of IFV, CPSV, and Phan (Table S4; Figure 1).
CPSV, which was not recognized in IFV.
Based on the previous study [52], Phan [53] classified all species of ferns from Vietnam, but not including lycophytes, into 135 genera, 28 families, 11 orders, and 4 classes, of which 3 families (Lindsaeaceae, Cibotaceae, and Lygodiaceae) are newly circumscribed for Vietnam (Tables S1 and S4). The results showed that Ophioglossaceae belonging to Polypodiophyta was transferred to another class, Psilotopsida; especially Marattiaceae belonging to Polypodiophyta was split into its own class, namely, Marattiopsida. Three families sensu IFV and CPSV were merged with other families in Phan, suggesting that the circumscription of these three families is broader than the corresponding families recognized in IFV and CPSV. Indeed, based on chloroplast sequence data, some families, sensu IFV and CPSV, were merged in Phan, and are apparently monophyletic, but nested within other families, e.g., Azollaceae (in Salviniaceae [54]) and Cheiropleuriaceae (in Dipteridaceae [55]).
According to PPG I [9], the lycophytes and ferns of Vietnam were classified into 2 classes, 3 sub-classes, 14 orders, 37 families, and 134 genera. By following this modern classification, the families of lycophytes and ferns in Vietnam are more than the previous treatments [2,17,53], of which six families (Cystopteridaceae, Rhachidosaraceae, Diplaziopsidaceae, Didymochlaenaceae, Hypodematiaceae, and Nephrolepidaceae) were newly circumscribed for Flora of Vietnam, but its number of genera is less than those of IFV, CPSV, and Phan (Table S4; Figure 1). The delimitation of families and genera of lycophytes and ferns in Vietnam according to IFV and CPSV is significantly different from those of PPG I, while Phan's treatment is mostly the same as PPG I. Some minor changes come from Acystopteris, Rhachidosorus, and Diplaziopsis (Woodsiaceae in Phan), which were transferred to Cystopteridaceae, Rhachidosoraceae, and Diplaziopsidaceae, respectively; Athyrium, Deparia, and Diplazium (Woodsiaceae in CPSV and Phan) were transferred to Athyriaceae; Didymochlaena (Dryopteridaceae in IFV, CPSV, and Phan) was transferred to Didymochlaenaceae; Hypodematium (Woodsiaceae in CPSV or Dryopteridaceae in Phan) and Leucostegia (Davalliaceae in IFV, CPSV, or Dryopteridaceae in Phan) were transferred to Hypodematiaceae; Nephrolepis (Davalliaceae in IFV or Oleandraceae in CPSV or Lomariopsidaceae in Phan) was transferred to Nephrolepidaceae (Table S4).

Gymnosperms
For the gymnosperms of Vietnam (Tables S2 and S5), IFV (Vol. 1) recognized 25 genera and 10 families, while CPSV (Vol. 1) identified 22 genera and 9 families, of which Araucariaceae was not recognized in CPSV. The delimitation of genera and families of gymnosperms in Vietnam in both IFV and CPSV is the same, with eight out of the nine families of gymnosperms in IFV having the exact same delimitation as CPSV (Tables S2  and S5). The significant difference between IFV and CPSV comes from the delimitation of Amentotaxus, which was placed in Amentotaxaceae in IFV, while CPSV transferred it to Taxaceae (Tables S2 and S5). The recognition of Amentotaxus in Taxaceae is in line with molecular study [58].
In the book Conifers of Vietnam, Nguyen & Thomas [59] presented 33 native conifer species of Vietnam, which were classified into 19 genera and 5 families, of which 3 previously recognized genera, i.e., Pseudotsuga (Pinaceae), Taiwania and Xanthocyparis (Cupressaceae), were added to the gymnosperms in Vietnam, but transferred Cunninghamia and Glyptostrobus (in Taxodiaceae sensu IFV and CPSV) to Cupressaceae based on the previous study [60], which merged Taxodiaceae into Cupressaceae.
According to GPG [10], the gymnosperms of Vietnam were classified into 4 sub-classes, 6 orders, 8 families, and 23 genera (Table S5). By following this modern classification, the families of gymnosperms in Vietnam are less than the previous treatments [2,17] (Table S5, Figure 2), of which nine genera in IFV, CPSV, and Nguyen & Thomas [2,17,59] have the exact delimitation with those in GPG (Table S5). The delimitation of Cupressaceae and Taxaceae sensu IFV, CPSV, and Nguyen & Thomas has remarkable changes in comparison with those in GPG, of which Glyptostrobus and Cunninghamia (Taxodiaceae) were transferred to Cupressaceae; Xanthocyparis (Cupressaceae), a genus endemic to Vietnam [60], was assigned to be a synonym for Cunninghamia (Cupressaceae); while Cephalotaxus (Cephalotaxaceae) and Amentotaxus (Amentotaxaceae) were transferred to Taxaceae.

Angiosperms
For the angiosperms of Vietnam (Tables S3, S6 and
According to APG IV [8], the angiosperms of Vietnam were classified into 246 families and 54 orders of 6 groups (basal angiosperms, magnoliids, Chlorantheles, monocots, Ceratophyllales, and eudicots). The number of families is more than those of IFV (238 families), but the number of families is less than those of CPSV (265 families). Of these, 203 and 225 families were also recognized in IFV and CPSV, respectively. Of the 199 families identified in IFV, CPSV, and APG IV, 133 families in IFV and CPSV have the exact delimitation as in the APG IV classification (Tables S6 and S7).
Linear classification of angiosperms in Vietnam following APG IV is presented in Table S7. Below are summaries of classifications of basal angiosperms, magnoliids, Chlorantheles, monocots, Ceratophyllales, and eudicots in IFV, CPSV, and APG IV.
Basal angiosperms: IFV and CPSV recognized five families (Cabombaceae, Nymphaeaceae, Barclayaceae, Ceratophyllaceae, and Nulumbonaceae) in the basal angiosperms, which include Amborellales, Nymphaeales, and Austrobaileyales (called as the ANA group), of which only Cabombaceae sensu IFV and CPSV has the exact delimitation as APG IV, while Barclayaceae was placed in Nymphaeaceae and Ceratophyllaceae (Ceratophyllales) was placed in the independent order in APG IV, which is the probable sister of eudicots. Nulumbonaceae was placed in the eudicot order Proteales. Furthermore, Illiciaceae and Schisandraceae were placed in the eudicot (Magnoliopsida) sensu IFV and CPSV and transferred to the order of Austrobaileyales in APG IV. Therefore, the basal angiosperms in Vietnam include two orders and three families, according to APG IV. The order Austrobai-leyales has not yet been circumscribed for Flora of Vietnam from the previous treatments (Table S7).
Magnoliids: The classification of magnoliids in Vietnam has been less controversial. The same nine families of magnoliids of Vietnam sensu IFV were also recognized in CPSV and APG IV, i.e., Saururaceae, Piperaceae, Aristolochiaceae, Myristicaceae, Magnoliaceae, Annonaceae, Hernandiaceae, Monimiaceae, and Lauraceae. However, Calycanthaceae was not recognized in IFV, but identified in both CPSV and APG IV. The delimitation of Magnoliales sensu CPSV and APG IV is the same, which includes Myristicaceae, Magnoliaceae, and Annonaceae. In contrast, the delimitation of some other families sensu CPSV is different from those of APG IV. Aristolochiaceae and Rafflesiaceae sensu CPSV were placed in Aristolochiales. However, APG IV placed Aristolochiaceae, together with Saururaceae and Piperaceae, in Piperales, and Rafflesiaceae was placed in Malpighiales (Eudicots). Laurales sensu CPSV includes five families, i.e., Calycantaceae, Hernandiaceae, Monimiaceae, Lauraceae, and Chloranthaceae, which are the same as APG IV, except for Chloranthaceae, which is an independent lineage and placed in the own order Chloranthales. Therefore, the magnoliids in Vietnam include ten families and three orders, according to APG IV (Table S7).
Chloranthales: Only one family, Chloranthaceae, was recognized. Wickett et al. [61] did not support the sister group with Magnoliids. Therefore, APG IV placed the order as an independent lineage with the remaining lineages (Magnoliids and Eudicots/Monocots/ Ceratophyllaceae). However, Chloranthaceae sensu IFV and CPSV were placed in the order Laurales.
Ceratophyllales: The independent lineage sensu APG IV containing only one order, Ceratophyllales, is the probable sister of eudicots. The order Ceratophyllales has only one family, Ceratophyllaceae, which was also recognized in both IFV and CPSV. Still, it was Supplementary Materials: The following supporting information can be downloaded at: https: //www.mdpi.com/article/10.3390/plants12040967/s1, Table S1: Comparison of classifications of lycophyte and fern families of Vietnam in IFV and CPSV; Table S2: Comparison of classifications of gymnosperm families of Vietnam in IFV and CPSV; Table S3: Comparison of classifications of angiosperm families of Vietnam in IFV and CPSV; Table S4: Classification of lycophytes and ferns of Vietnam according to the PPG 1 classification system; Table S5: Classification of gymnosperms of Vietnam according to the GPG classification system; Table S6: Comparison of angiosperm families of Vietnam following IFV, CPSV, and APG IV; Table S7: Classification of angiosperm families of Vietnam according to the APG IV classification system.

Data Availability Statement:
The study did not report any additional data.